Cholinergic synapses in the central nervous system: studies of the immunocytochemical localization of choline acetyltransferase
Abstract
Cholinergic synapses can be identified in immunocytochemical preparations by the use of monoclonal antibodies and specific antisera to choline acetyltransferase (ChAT), the synthesizing enzyme for acetylcholine (ACh) and a specific marker for cholinergic neurons. Electron microscopic studies demonstrate that the fibers and varicosities observed in light microscopic preparations of many brain regions are small-diameter unmyelinated axons and vesicle-containing boutons. The labeled boutons generally contain clear vesicles and one or more mitochondrial profiles. Many of these boutons form synaptic contacts, and the synapses are frequently of the symmetric type, displaying thin postsynaptic densities and relatively short contact zones. However, ChAT-labeled synapses with asymmetric junctions are also observed, and their frequency varies among different brain regions. Unlabeled dendritic shafts are the most common postsynaptic elements in virtually all regions examined although other neuronal elements, including dendritic spines and neuronal somata, also receive some cholinergic innervation. ChAT-labeled boutons form synaptic contacts with several different types of unlabeled neurons within the same brain region. Such findings are consistent with a generally diffuse pattern of cholinergic innervation in many parts of the central nervous system. Despite many similarities in the characteristics of ChAT-labeled synapses, there appears to be some heterogeneity in the cholinergic innervation within as well as among brain regions. Differences are observed in the sizes of ChAT-immunoreactive boutons, the types of synaptic contacts, and the predominant postsynaptic elements. Thus, the cholinergic system presents interesting challenges for future studies of the morphological organization and related function of cholinergic synapses.
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There is an anatomical mismatch between the sites of acetylcholine release and the location of cholinergic receptors.
“There is an anatomical mismatch between the sites of ACh release (Houser, 1990; Wainer et al., 1984a; Wainer et al., 1984b) and the location of cholinergic receptors (Arroyo-Jimenez et al., 1999; Hill Jr. et al., 1993; Kawai et al., 2007).”
From Acetylcholine as a Neuromodulator: Cholinergic Signaling Shapes Nervous System Function and Behavior (2012) · cites this paper as Houser, 1990
Cites
Central cholinergic pathways in the rat: An overview based on an alternative nomenclature (Ch1–Ch6)
Mesulam, M. M., Mufson, E. J., Wainer, B. H., & Levey, A. I. (1983) · Neuroscience · doi:10.1016/0306-4522(83)90108-2 · Cited by 2,329 · see citing works
Mesulam, M. ‐., Mufson, E. J., Levey, A. I., & Wainer, B. H. (1983) · Journal of Comparative Neurology · doi:10.1002/cne.902140206 · Cited by 1,962 · see citing works
(1976) · Medical Entomology and Zoology · Cited by 1,328 · see citing works
Armstrong, D. M., Saper, C. B., Levey, A. I., Wainer, B. H., & Terry, R. D. (1983) · The Journal of Comparative Neurology · doi:10.1002/cne.902160106 · Cited by 970 · see citing works
The organization and some projections of cholinergic neurons of the mammalian forebrain
Fibiger, H. C. (1982) · Brain Research Reviews · doi:10.1016/0165-0173(82)90011-x · Cited by 818 · see citing works
Houser, C. R., Crawford, G. D., Barber, R. P., Salvaterra, P. M., & Vaughn, J. E. (1983) · Brain Research · doi:10.1016/0006-8993(83)91312-4 · Cited by 748 · see citing works
Amaral, D. G., & Kurz, J. (1985) · The Journal of Comparative Neurology · doi:10.1002/cne.902400104 · Cited by 687 · see citing works
GABA neurons are the major cell type of the nucleus reticularis thalami
Houser, C. R., Vaughn, J. E., Barber, R. P., & Roberts, E. (1980) · Brain Research · doi:10.1016/0006-8993(80)90925-7 · Cited by 668 · see citing works
Woolf, N. J., & Butcher, L. L. (1986) · Brain Research Bulletin · doi:10.1016/0361-9230(86)90134-6 · Cited by 668 · see citing works
Frotscher, M., & Léránth, C. (1985) · The Journal of Comparative Neurology · doi:10.1002/cne.902390210 · Cited by 600 · see citing works
The origins of cholinergic and other subcortical afferents to the thalamus in the rat
Hallanger, A. E., Levey, A. I., Lee, H. J., Rye, D. B., & Wainer, B. H. (1987) · The Journal of Comparative Neurology · doi:10.1002/cne.902620109 · Cited by 595 · see citing works
Mechanisms of action of acetylcholine in the guinea‐pig cerebral cortex in vitro.
McCormick, D. A., & Prince, D. A. (1986) · The Journal of Physiology · doi:10.1113/jphysiol.1986.sp016112 · Cited by 499 · see citing works
Bolam, J. P., Wainer, B. H., & Smith, A. D. (1984) · Neuroscience · doi:10.1016/0306-4522(84)90165-9 · Cited by 485 · see citing works
Evidence for a cholinergic projection to neocortex from neurons in basal forebrain.
Johnston, M. V., McKinney, M., & Coyle, J. T. (1979) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.76.10.5392 · Cited by 460 · see citing works
A POST-MORTEM STUDY OF THE CHOLINERGIC AND GABA SYSTEMS IN SENILE DEMENTIA
Rossor, M. N., Garrett, N., Johnson, A. L., Mountjoy, C. Q., Roth, M., & Iversen, L. L. (1982) · Brain · doi:10.1093/brain/105.2.313 · Cited by 460 · see citing works
Barber, R. P., Phelps, P. E., Houser, C. R., Crawford, G. D., Salvaterra, P. M., & Vaughn, J. E. (1984) · The Journal of Comparative Neurology · doi:10.1002/cne.902290305 · Cited by 453 · see citing works
Eckenstein, F. P., & Thoenen, H. (1982) · The EMBO Journal · doi:10.1002/j.1460-2075.1982.tb01175.x · Cited by 442 · see citing works
Neocortical cholinergic innervation: A description of extrinsic and intrinsic components in the rat
Johnston, M. V., McKinney, M., & Coyle, J. T. (1981) · Experimental Brain Research · doi:10.1007/bf00237760 · Cited by 441 · see citing works
Cholinergic neurons of the laterodorsal tegmental nucleus: Efferent and afferent connections
Satoh, K., & Fibiger, H. C. (1986) · The Journal of Comparative Neurology · doi:10.1002/cne.902530302 · Cited by 440 · see citing works
McCormick, D. A., & Prince, D. A. (1986) · Nature · doi:10.1038/319402a0 · Cited by 398 · see citing works
Phelps, P. E., Houser, C. R., & Vaughn, J. E. (1985) · The Journal of Comparative Neurology · doi:10.1002/cne.902380305 · Cited by 396 · see citing works
Houser, C. R., Crawford, G. D., Salvaterra, P. M., & Vaughn, J. E. (1985) · The Journal of Comparative Neurology · doi:10.1002/cne.902340103 · Cited by 395 · see citing works
Cholinergic modulation of the functional organization of the cat visual cortex
Sillito, A. M., & Kemp, J. A. (1983) · Brain Research · doi:10.1016/0006-8993(83)90015-x · Cited by 387 · see citing works
Acetylcholine Mediates a Slow Synaptic Potential in Hippocampal Pyramidal Cells
Cole, A. E., & Nicoll, R. A. (1983) · Science · doi:10.1126/science.6612345 · Cited by 374 · see citing works
Biology of cholinergic function
Silver, A. (1977) · Neuroscience · doi:10.1016/0306-4522(77)90041-0 · Cited by 369 · see citing works
Eckenstein, F., & Baughman, R. W. (1984) · Nature · doi:10.1038/309153a0 · Cited by 356 · see citing works
Hoover, D. B., Muth, E. A., & Jacobowitz, D. M. (1978) · Brain Research · doi:10.1016/0006-8993(78)90408-0 · Cited by 308 · see citing works
Two types of muscarinic response to acetylcholine in mammalian cortical neurons.
McCormick, D. A., & Prince, D. A. (1985) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.82.18.6344 · Cited by 302 · see citing works
Sofroniew, M. V., Priestley, J. V., Consolazione, A., Eckenstein, F. P., & Cuello, A. C. (1985) · Brain Research · doi:10.1016/0006-8993(85)90527-x · Cited by 293 · see citing works
Cholinergic systems in mammalian brain identified with antibodies against choline acetyltransferase
Wainer, B. H., Levey, A. I., Mufson, E. J., & Mesulam, M. M. (1984) · Neurochemistry International · doi:10.1016/0197-0186(84)90089-5 · Cited by 287 · see citing works
Oertel, W. H., & Mugnaini, E. (1984) · Neuroscience Letters · doi:10.1016/0304-3940(84)90519-6 · Cited by 282 · see citing works
Levey, A. I., Wainer, B. H., Rye, D. B., Mufson, E. J., & Mesulam, M. M. (1984) · Neuroscience · doi:10.1016/0306-4522(84)90234-3 · Cited by 276 · see citing works
Carlsen, J., Záborszky, L., & Heimer, L. (1985) · The Journal of Comparative Neurology · doi:10.1002/cne.902340203 · Cited by 271 · see citing works
Levey, A. I., Armstrong, D. M., Atweh, S., Terry, R. D., & Wainer, B. (1983) · Journal of Neuroscience · doi:10.1523/jneurosci.03-01-00001.1983 · Cited by 268 · see citing works
GABA Neurons in the Cerebral Cortex
Houser, C. R., Vaughn, J. E., Hendry, S. H. C., Jones, E. G., & Peters, A. (1984) · Cerebral cortex · doi:10.1007/978-1-4615-6610-6_3 · Cited by 261 · see citing works
Yen, C., Conley, M., Hendry, S., & Jones, E. G. (1985) · Journal of Neuroscience · doi:10.1523/jneurosci.05-08-02254.1985 · Cited by 258 · see citing works
Z�borszky, L., Heimer, L., Eckenstein, F. P., & Leranth, C. (1986) · The Journal of Comparative Neurology · doi:10.1002/cne.902500303 · Cited by 249 · see citing works
Woolf, N. J., & Butcher, L. L. (1982) · Brain Research Bulletin · doi:10.1016/0361-9230(82)90102-2 · Cited by 231 · see citing works
Woolf, N. J., & Butcher, L. L. (1981) · Brain Research Bulletin · doi:10.1016/0361-9230(81)90004-6 · Cited by 221 · see citing works
Wainer, B. H., Bolam, J. P., Freund, T. F., Henderson, Z., Totterdell, S., & Smith, A. D. (1984) · Brain Research · doi:10.1016/0006-8993(84)90918-1 · Cited by 213 · see citing works
Oertel, W., Graybiel, A. M., Mugnaini, E., Elde, R., Schmechel, D. E., & Kopin, I. J. (1983) · Journal of Neuroscience · doi:10.1523/jneurosci.03-06-01322.1983 · Cited by 212 · see citing works
The anatomy of the CNS cholinergic neurons
Cuello, A. C., & Sofroniew, M. V. (1984) · Trends in Neurosciences · doi:10.1016/s0166-2236(84)80161-7 · Cited by 212 · see citing works
Bruce, G., Wainer, B. H., & Hersh, L. B. (1985) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.1985.tb04030.x · Cited by 206 · see citing works
Somogyi, P., & Smith, A. D. (1979) · Brain Research · doi:10.1016/0006-8993(79)90084-2 · Cited by 203 · see citing works
Eckenstein, F. P., & Thoenen, H. (1983) · Neuroscience Letters · doi:10.1016/0304-3940(83)90002-2 · Cited by 198 · see citing works
Steriade, M., Parent, A., Paré, D., & Smith, Y. (1987) · Brain Research · doi:10.1016/0006-8993(87)90408-2 · Cited by 194 · see citing works
Cholinergic innervation of hippocampal GAD‐ and somatostatin‐immunoreactive commissural neurons
Léránth, C., & Frotscher, M. (1987) · The Journal of Comparative Neurology · doi:10.1002/cne.902610104 · Cited by 189 · see citing works
Seizure-related brain damage induced by cholinergic agents
Olney, J. W., de Gubareff, T., & Labruyere, J. (1983) · Nature · doi:10.1038/301520a0 · Cited by 187 · see citing works
Choline acetyltransferase content of limbic nuclei of the rat
Palkovits, M., Saavedra, J. M., Kobayashi, R. M., & Brownstein, M. (1974) · Brain Research · doi:10.1016/0006-8993(74)90442-9 · Cited by 185 · see citing works
Frotscher, M., & Léránth, C. (1986) · The Journal of Comparative Neurology · doi:10.1002/cne.902430106 · Cited by 179 · see citing works
Ribak, C., Bradurne, R., & Harris, A. B. (1982) · Journal of Neuroscience · doi:10.1523/jneurosci.02-12-01725.1982 · Cited by 176 · see citing works
The cholinergic innervation of the visual thalamus: an EM immunocytochemical study
Dolabela, A. D. L., Montero, V. M., & Singer, W. (1985) · Experimental Brain Research · doi:10.1007/bf00237681 · Cited by 147 · see citing works
Production of specific antibodies to choline acetyltransferase purified from pig brain
Eckenstein, F. P., Barde, Y., & Thoenen, H. (1981) · Neuroscience · doi:10.1016/0306-4522(81)90065-8 · Cited by 141 · see citing works
Synaptic organization of cholinergic neurons in the monkey neostriatum
DiFiglia, M. (1987) · The Journal of Comparative Neurology · doi:10.1002/cne.902550208 · Cited by 141 · see citing works
Cholinergic projections from the basal forebrain of rat to the amygdala
Nagai, T., Kimura, H., Maeda, T., McGeer, P., Peng, F., & McGeer, E. (1982) · The Journal of Neuroscience · doi:10.1523/jneurosci.02-04-00513.1982 · Cited by 140 · see citing works
Montero, V. M., & Singer, W. (1984) · Experimental Brain Research · doi:10.1007/bf00237447 · Cited by 135 · see citing works
Choline acetyltransferase immunoreactivity in the rat thalamus
Levey, A. I., Hallanger, A. E., & Wainer, B. H. (1987) · The Journal of Comparative Neurology · doi:10.1002/cne.902570302 · Cited by 134 · see citing works
Ingham, C. A., Bolam, J. P., Wainer, B. H., & Smith, A. D. (1985) · The Journal of Comparative Neurology · doi:10.1002/cne.902390205 · Cited by 127 · see citing works
Connaughton, M., Priestley, J. V., Sofroniew, M. V., Eckenstein, F. P., & Cuello, A. C. (1986) · Neuroscience · doi:10.1016/0306-4522(86)90237-x · Cited by 127 · see citing works
Interaction of monoclonal antibodies with mammalian choline acetyltransferase.
Crawford, G. D., Correa, L., & Salvaterra, P. M. (1982) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.79.22.7031 · Cited by 126 · see citing works
Białowas, J., & Frotscher, M. (1987) · The Journal of Comparative Neurology · doi:10.1002/cne.902590209 · Cited by 123 · see citing works
Matthews, D. A., Salvaterra, P. M., Crawford, G. D., Houser, C. R., & Vaughn, J. E. (1987) · Brain Research · doi:10.1016/0006-8993(87)91044-4 · Cited by 121 · see citing works
Triller, A., & Korn, H. (1982) · Journal of Neurophysiology · doi:10.1152/jn.1982.48.3.708 · Cited by 119 · see citing works
Clarke, D. J., Gage, F. H., & Björklund, A. (1986) · Brain Research · doi:10.1016/0006-8993(86)90523-8 · Cited by 119 · see citing works
Lamour, Y. A., Dutar, P., & Jobert, A. (1982) · Neuroscience · doi:10.1016/0306-4522(82)90259-7 · Cited by 115 · see citing works
Somatostatin selectively enhances acetylcholine-induced excitations in rat hippocampus and cortex.
Mancillas, J. R., Siggins, G. R., & Bloom, F. E. (1986) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.83.19.7518 · Cited by 114 · see citing works
Clarke, D. J. (1985) · Brain Research · doi:10.1016/0006-8993(85)91253-3 · Cited by 112 · see citing works
Emson, P. C., Paxinos, G., Salle, G. L. G. L., Ben‐Ari, Y., & Silver, A. (1979) · Brain Research · doi:10.1016/0006-8993(79)90559-6 · Cited by 110 · see citing works
Phelps, P. E., & Vaughn, J. E. (1986) · Journal of Neurocytology · doi:10.1007/bf01611860 · Cited by 106 · see citing works
Cholinergic neurons and fibres in the rat visual cortex
Parnavelas, J. G., Kelly, W. L., Franke, E., & Eckenstein, F. P. (1986) · Journal of Neurocytology · doi:10.1007/bf01611435 · Cited by 103 · see citing works
de Lima, A. D., & Singer, W. (1986) · The Journal of Comparative Neurology · doi:10.1002/cne.902500306 · Cited by 92 · see citing works
Armstrong, D. M. (1986) · The Journal of Comparative Neurology · doi:10.1002/cne.902500108 · Cited by 91 · see citing works
Anderson, K. J., Gibbs, R. B., Salvaterra, P. M., & Cotman, C. W. (1986) · The Journal of Comparative Neurology · doi:10.1002/cne.902490211 · Cited by 89 · see citing works
Carlsen, J., & Heimer, L. (1986) · The Journal of Comparative Neurology · doi:10.1002/cne.902440110 · Cited by 84 · see citing works
Rovira, C., Ben‐Ari, Y., CherubiniP, E., Krnjević, K., & Ropert, N. (1983) · Neuroscience · doi:10.1016/0306-4522(83)90028-3 · Cited by 77 · see citing works
Takagi, H., Somogyi, P., & Smith, A. D. (1984) · Journal of Neurocytology · doi:10.1007/bf01148118 · Cited by 72 · see citing works
Dodt, H. U., & Misgeld, U. (1986) · The Journal of Physiology · doi:10.1113/jphysiol.1986.sp016304 · Cited by 71 · see citing works
Clarke, D. J., & Dunnett, S. B. (1986) · The Journal of Comparative Neurology · doi:10.1002/cne.902500206 · Cited by 68 · see citing works
Hellendall, R. P., Godfrey, D. A., Ross, C. D., Armstrong, D. M., & Price, J. L. (1986) · The Journal of Comparative Neurology · doi:10.1002/cne.902490405 · Cited by 65 · see citing works
Eckenrode, T. C., Barr, G. A., Battisti, W. P., & Murray, M. (1987) · Brain Research · doi:10.1016/0006-8993(87)90095-3 · Cited by 64 · see citing works
Stichel, C. C., & Singer, W. (1987) · The Journal of Comparative Neurology · doi:10.1002/cne.902580107 · Cited by 63 · see citing works
Clarke, D. J., Gage, F. H., Nilsson, O., & Björklund, A. (1986) · The Journal of Comparative Neurology · doi:10.1002/cne.902520405 · Cited by 57 · see citing works
Mechanisms of Transmitter Action in the Vertebrate Central Nervous System
Siggins, G. R., & Gruol, D. L. (1986) · Comprehensive physiology · doi:10.1002/cphy.cp010401 · Cited by 53 · see citing works
Dinopoulos, A., Parnavelas, J. G., & Eckenstein, F. P. (1986) · Journal of Neurocytology · doi:10.1007/bf01611861 · Cited by 45 · see citing works
Species-specific second antibodies reduce spurious staining in immunocytochemistry.
Houser, C. R., Barber, R. P., Crawford, G. D., Matthews, D. A., Phelps, P. E., Salvaterra, P. M., & Vaughn, J. E. (1984) · Journal of Histochemistry & Cytochemistry · doi:10.1177/32.4.6368679 · Cited by 38 · see citing works
Acetylcholine as an Excitatory and Inhibitory Transmitter in the Mammalian Central Nervous System
Kelly, J. S., Dodd, J., & Dingledine, R. J. (1979) · Progress in brain research · doi:10.1016/s0079-6123(08)64638-5 · Cited by 34 · see citing works
Lenn, N. J., Léránth, C., & Záborszky, L. (1986) · Journal of Neurocytology · doi:10.1007/bf01611866 · Cited by 29 · see citing works
Lenn, N. J., Léránth, C., & Záborszky, L. (1985) · Journal of Neurocytology · doi:10.1007/bf01224804 · Cited by 27 · see citing works
A search for choline acetyltransferase-like immunoreactivity in neurons of cat striate cortex
Stichel, C. C., de Lima, A. D., & Singer, W. (1987) · Brain Research · doi:10.1016/0006-8993(87)90313-1 · Cited by 21 · see citing works
Brady, D. R., & Vaughn, J. E. (1988) · Neuroscience · doi:10.1016/0306-4522(88)90083-8 · Cited by 18 · see citing works
Kelly, J. S., & Rogawski, M. A. (1985) · Springer eBooks · doi:10.1007/978-1-4684-4961-7_6 · Cited by 12 · see citing works
Flagged first, then by citations
1 of the 92 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
Acetylcholine as a Neuromodulator: Cholinergic Signaling Shapes Nervous System Function and Behavior
Picciotto, M. R., Higley, M. J., & Mineur, Y. S. (2012) · Neuron · doi:10.1016/j.neuron.2012.08.036 · Cited by 1,404 · see citing works
(2013) · Elsevier eBooks · doi:10.1016/c2010-0-65035-8 · Cited by 465 · see citing works
Diffuse transmission by acetylcholine in the CNS
Descarries, L., Gisiger, V., & Steriade, M. (1997) · Progress in Neurobiology · doi:10.1016/s0301-0082(97)00050-6 · Cited by 406 · see citing works
Dye-doped nanoparticles for bioanalysis
Yan, J., Estévez, M. ‐., Smith, J. E., Wang, K., He, X., Wang, L., & Tan, W. (2007) · Nano Today · doi:10.1016/s1748-0132(07)70086-5 · Cited by 378 · see citing works
Ultrasensitive detection of biomolecules with fluorescent dye-doped nanoparticles
Lian, W., Litherland, S. A., Badrane, H., Tan, W., Wu, D., Baker, H. V., Gulig, P. A., Lim, D. V., & Jin, S. (2004) · Analytical Biochemistry · doi:10.1016/j.ab.2004.08.005 · Cited by 270 · see citing works
Descarries, L., & Mechawar, N. (2000) · Progress in brain research · doi:10.1016/s0079-6123(00)25005-x · Cited by 241 · see citing works
Umbriaco, D., Watkins, K. C., Descarries, L., Cozzari, C., & Hartman, B. K. (1994) · The Journal of Comparative Neurology · doi:10.1002/cne.903480304 · Cited by 237 · see citing works
Umbriaco, D., Garcia, S., Beaulieu, C., & Descarries, L. (1995) · Hippocampus · doi:10.1002/hipo.450050611 · Cited by 199 · see citing works
Cicchetti, F., Prensa, L., Wu, Y., & Parent, A. (2000) · Brain Research Reviews · doi:10.1016/s0165-0173(00)00039-4 · Cited by 192 · see citing works
Ultrastructural characterization of the acetylcholine innervation in adult rat neostriatum
Contant, C., Umbriaco, D., Garcia, S., Watkins, K. C., & Descarries, L. (1996) · Neuroscience · doi:10.1016/0306-4522(95)00507-2 · Cited by 175 · see citing works
Chapter 5 Cholinergic innervation and receptors in the cerebellum
Jaarsma, D., Ruigrok, T. J. H., Caffé, R., Cozzari, C., Levey, A. I., Mugnaini, E., & Voogd, J. (1997) · Progress in brain research · doi:10.1016/s0079-6123(08)63359-2 · Cited by 169 · see citing works
Developmental aspects of the cholinergic system
Abreu‐Villaça, Y., Filgueiras, C. C., & Manhães, A. C. (2010) · Behavioural Brain Research · doi:10.1016/j.bbr.2009.12.049 · Cited by 166 · see citing works
Cholinergic innervation of the human thalamus: Dual origin and differential nuclear distribution
Heckers, S., Geula, C., & Mesulam, M. M. (1992) · The Journal of Comparative Neurology · doi:10.1002/cne.903250107 · Cited by 132 · see citing works
Sprouting in the hippocampus is layer-specific
Frotscher, M., Heimrich, B., & Deller, T. (1997) · Trends in Neurosciences · doi:10.1016/s0166-2236(96)01018-1 · Cited by 109 · see citing works
Selden, N. R. W., Geula, C., Hersh, L. B., & Mesulam, M. M. (1994) · Neuroscience · doi:10.1016/0306-4522(94)90491-x · Cited by 106 · see citing works
Fu, D., Yang, W., & Xie, X. S. (2016) · Journal of the American Chemical Society · doi:10.1021/jacs.6b10727 · Cited by 103 · see citing works
Conner, J. M., & Varon, S. S. (1992) · The Journal of Comparative Neurology · doi:10.1002/cne.903260304 · Cited by 76 · see citing works
Ikonomović, M. D., Abrahamson, E. E., Isanski, B. A., Wuu, J., Mufson, E. J., & DeKosky, S. T. (2007) · Archives of Neurology · doi:10.1001/archneur.64.9.1312 · Cited by 71 · see citing works
Parent, M., & Descarries, L. (2008) · The Journal of Comparative Neurology · doi:10.1002/cne.21868 · Cited by 64 · see citing works
Bellier, J., & Kimura, H. (2007) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2007.04458.x · Cited by 62 · see citing works
Woolf, N. J. (1996) · Neuroscience · doi:10.1016/0306-4522(96)00163-7 · Cited by 62 · see citing works
The hypothesis of an ambient level of acetylcholine in the central nervous system
Descarries, L. (1998) · Journal of Physiology-Paris · doi:10.1016/s0928-4257(98)80013-2 · Cited by 58 · see citing works
Muller, J. F., Mascagni, F., & McDonald, A. J. (2010) · The Journal of Comparative Neurology · doi:10.1002/cne.22550 · Cited by 49 · see citing works
Jeune, H. L., & Jourdan, F. (1993) · The Journal of Comparative Neurology · doi:10.1002/cne.903360209 · Cited by 48 · see citing works
Avendaño, C., Umbriaco, D., Dykes, R. W., & Descarries, L. (1996) · Journal of Chemical Neuroanatomy · doi:10.1016/0891-0618(96)00132-9 · Cited by 42 · see citing works
Development of DNA aptamers for cytochemical detection of acetylcholine
Bruno, J. G., Carrillo, M. P., Phillips, T., & King, B. G. (2008) · In Vitro Cellular & Developmental Biology - Animal · doi:10.1007/s11626-008-9086-0 · Cited by 35 · see citing works
Muller, J. F., Mascagni, F., Zaric, V., & McDonald, A. J. (2013) · The Journal of Comparative Neurology · doi:10.1002/cne.23254 · Cited by 34 · see citing works
Fine structural features of the acetylcholine innervation in the developing neostriatum of rat
Aznavour, N., Mechawar, N., Watkins, K. C., & Descarries, L. (2003) · The Journal of Comparative Neurology · doi:10.1002/cne.10660 · Cited by 30 · see citing works
Woolf, N. J. (1993) · Journal of Chemical Neuroanatomy · doi:10.1016/0891-0618(93)90012-s · Cited by 30 · see citing works
Gonzalo‐Ruiz, A., Sanz-Anquela, M., & Lieberman, A. R. (1995) · Anatomy and Embryology · doi:10.1007/bf00710103 · Cited by 27 · see citing works
Nanomedicine and Early Cancer Diagnosis: Molecular Imaging using Fluorescence Nanoparticles
Jin, K., Yao, J., Ying, X., Lin, Y., & Chen, Y. (2020) · Current Topics in Medicinal Chemistry · doi:10.2174/1568026620666200922112640 · Cited by 26 · see citing works
Heimrich, B., & Frotscher, M. (1993) · Neuroscience · doi:10.1016/0306-4522(93)90531-j · Cited by 26 · see citing works
Neurotransmitters and receptors in the dorsal horn of the spinal cord
Budai, D. (2000) · Acta Biologica Szegediensis · Cited by 25 · see citing works
Phelps, P. E., Houser, C. R., & Vaughn, J. E. (1992) · Neuroscience · doi:10.1016/0306-4522(92)90343-z · Cited by 23 · see citing works
Wei, Z., Wei, M., Yang, X., Xu, Y., Gao, S., & Ren, K. (2022) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2022/9176923 · Cited by 24 · see citing works
Henselmans, J. M. L., & Wouterlood, F. G. (1994) · The Journal of Comparative Neurology · doi:10.1002/cne.903450105 · Cited by 20 · see citing works
Pauža, D. H., Skripka, V., Paužienė, N., & Stropus, R. (1999) · The Anatomical Record · doi:10.1002/(sici)1097-0185(19990701)255:3 · Cited by 48 · see citing works
Kimura, S., Bellier, J., Matsuo, A., Tooyama, I., & Kimura, H. (2006) · Neurochemistry International · doi:10.1016/j.neuint.2006.08.011 · Cited by 19 · see citing works
Distler, P. G., & Robertson, R. T. (1993) · Journal of Neurocytology · doi:10.1007/bf01181489 · Cited by 19 · see citing works
Anglade, P., & Larabi, Y. (2010) · Biomedical Research · doi:10.2220/biomedres.31.1 · Cited by 16 · see citing works
Oda, S., Kuroda, M., Kakuta, S., Tanihata, S., Ishikawa, Y., & Kishi, K. (2003) · Brain Research Bulletin · doi:10.1016/s0361-9230(02)00964-4 · Cited by 15 · see citing works
Ha, D. H., Robertson, R. T., & Weiss, J. H. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-11-04201.1998 · Cited by 14 · see citing works
Yadollahpour, A., Rezaee, Z., Jalilifar, M., & Samaneh, R. (2014) · Material Science Research India · doi:10.13005/msri/110203 · Cited by 12 · see citing works
Immunolocalization of muscarinic receptor subtypes in the reticular thalamic nucleus of rats
Oda, S., Sato, F., Okada, A., Akahane, S., Igarashi, H., Yokofujita, J., Yang, J., & Kuroda, M. (2007) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2007.07.017 · Cited by 12 · see citing works
Wang, Q., Guan, J., Ochiai, H., & Nakai, Y. (1998) · Brain Research Bulletin · doi:10.1016/s0361-9230(98)00061-6 · Cited by 9 · see citing works
Asynaptic and Synaptic Innervation by Acetylcholine Neurons of the Central Nervous System
Descarries, L., & Parent, M. (2014) · Elsevier eBooks · doi:10.1016/b978-0-12-418675-0.00014-6 · Cited by 6 · see citing works
Toxicological effect of N , N , N ′, N ′-tetramethylethylene on rat brain acetylcholinesterase
Ahmed, M., Latif, N., Khan, R. A., Ahmad, A., Schetinger, M. R. C., & da Rocha, J. B. T. (2012) · Toxicology and Industrial Health · doi:10.1177/0748233712457443 · Cited by 3 · see citing works
Oda, S., Kuroda, M., Ger, Y., Ojima, H., Chen, S., & Kishi, K. (1998) · Brain Research · doi:10.1016/s0006-8993(98)00570-8 · Cited by 3 · see citing works
Cholinergic neurons in the motor areas of the human cerebral cortex
Okhotin, V. E., Калиниченко, С. Г., & Motavkin, P. A. (1999) · Neuroscience and Behavioral Physiology · doi:10.1007/bf02465331 · Cited by 3 · see citing works
Cholinergic Plasticity and the Meaning of Death
McKinney, M., Baskerville, K. A., Personett, D. A., Williams, K., & Gonzales, J. (2003) · Springer eBooks · doi:10.1007/978-1-4615-0282-1_2 · Cited by 3 · see citing works
FloDots for Bioimaging and Bioanalysis
Yao, G., Wu, Y., Schiavone, D. L., Wang, L., & Tan, W. (2008) · CRC Press eBooks · doi:10.1201/9781420007534-12
FloDots for Bioimaging and Bioanalysis
Wu, Y., Yao, G., Wang, L., Schiavone, D. L., & Tan, W. (2008) · CRC Press eBooks · doi:10.1201/9781420007534.ch12
Water Drinking Behavior Associated with Aversive Arousal in Rats: An Integrative Approach
Brudzyński, S. M. (2022) · Brain Sciences · doi:10.3390/brainsci13010060
- Authors
- Houser, C. R.
- Affiliations
- United States Department of Veterans Affairs (US)
- Corresponding author
- Houser, Carolyn R.
- ORCID
- Houser, Carolyn R.
- Venue
- Journal of Electron Microscopy Technique
- Publisher
- Wiley
- Published
- 1990-05
- Volume
- 15
- Issue
- 1
- Pages
- 2-19
- ISSN
- 0741-0581 (ISSN-L)
- 1553-0817
- OpenAlex
- W1968506805
- Cited by
- 55
- References
- 92
- Citations by year
- 2022: 2 · 2020: 1 · 2019: 1 · 2016: 1 · 2014: 2 · 2013: 2 · 2012: 2
- FWCI
- 0.30
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Journal of Electron Microscopy Technique (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Epilepsy Foundation
- National Institutes of Health (5p01ns021908-10)
- National Institute of Neurological Disorders and Stroke (NS-21908)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Nicotinic Acetylcholine Receptors Study
- Health Sciences › Medicine › Pharmacology › Cholinesterase and Neurodegenerative Diseases
- Keywords
- cholinergic synapses, choline acetyltransferase, acetylcholine, cholinergic neurons, synaptic ultrastructure, postsynaptic density, synaptic boutons, cholinergic innervation, central nervous system, synaptic heterogeneity, dendritic innervation
- MeSH terms
- Animals, Central Nervous System, Cerebral Cortex, Choline O-Acetyltransferase, Cholinergic Fibers, Corpus Striatum, Hippocampus, Humans, Immunohistochemistry, Microscopy, Electron, Spinal Cord, Synapses, Thalamus
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